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Accepted Article This article has been accepted for publication and undergone full peer review but has not been through the copyediting typesetting pagination and proofreading process which may lead to differences between this version and the Version of Record Please cite this article as doi 10 1111 tmi 12482 This article is protected by copyright All rights reserved Article Type Original article High prevalence of common respiratory viruses and no evidence of Middle East Respiratory Syn drome Coronavirus in Hajj pilgrims returning to Ghana 2013 Augustina Annan 1 Michael Owusu 1 Kwadwo Sarfo Marfo 1 Richard Larbi 1 Francisca Naana Sarpong 1 Yaw Adu Sarkodie 2 Joseph Amankwa 3 Samuel Fiafemetsi 4 Christian Drosten 5 6 Ellis Owusu Dabo 1 Isabella Eckerle 5 1 Kumasi Centre for Collaborative Research in Tropical Medicine Kwame Nkrumah University of Sci ence and Technology Kumasi Ghana 2 Department of Clinical Microbiology Kwame Nkrumah University of Science and Technology Ku masi Ghana 3 Public Health Division Ghana Health Services Accra Ghana 4 Port Health Division Ghana Health Services Accra Ghana 5 Institute of Virology University of Bonn Medical Centre Bonn Germany 6 German Centre for Infection Research Abstract Objective The Middle East respiratory syndrome coronavirus MERS CoV emerged in 2012 on the Arabian Peninsula and has caused severe respiratory disease with more than 800 laboratory confirmed cases The return of infected pilgrims to their home countries with a putative spread of MERS CoV necessitates further surveillance Methods A surveillance study of 839 adult African Hajj pilgrims returning to Accra in Ghana West Africa was conducted in 2013 to assess the prevalence of respiratory symptoms as well as of MERS CoV human Rhinovirus HRV Respiratory Syncytial Virus RSV and Influenza A virus FLU A infec tion Results 651 77 6 pilgrims had respiratory symptoms Tests were positive for at least one of the viruses other than MERS CoV in 179 21 3 of all pilgrims with 22 4 detection in symptomatic vs 17 6 detection in asymptomatic pilgrims No MERS CoV was detected although common respira tory viruses were prevalent with positive findings for HRV in 141 individuals 16 8 RSV in 43 indi Accepted Article This article is protected by copyright All rights reserved viduals 5 1 and FLU A in 11 individuals 1 3 Results were positive for more than one virus in 16 1 9 individuals including 14 1 7 RSV HRV co infections and 2 0 2 FLU A HRV co infections A total 146 22 4 of the symptomatic returnees tested positive for at least one respiratory virus compared with 33 17 6 of the asymptomatic pilgrims who had at least one detectable virus in their sample Conclusions The prevalence of viral respiratory infections among Hajj pilgrims in both symptomatic and asymptomatic subjects is high Although it is reassuring that MERS CoV was not detected in the tested cohort there is a need for active surveillance of Hajj pilgrims Keywords MERS Coronavirus respiratory illness Hajj pilgrimage Human rhinovirus Respiratory Syncytial virus Influenza A virus Introduction Coronaviruses CoV in the genera Alphacoronavirus and Betacoronavirus order Nidovirales family Coronaviridae subfamily Coronavirinae infect a broad range of mammalian species including hu mans Woo et al 2009 While the human CoVs HCoV HKU1 HCoV 229E HCoV NL63 and HCoV OC43 cause mild to moderate respiratory tract infection an epidemic of severe lower respiratory tract infections with a case fatality rate of approximately 10 was caused by SARS CoV in 2002 2004 Drosten et al 2003 In 2012 a novel coronavirus termed Middle East Respiratory Syndrome CoV MERS CoV emerged on the Arabian Peninsula MERS CoV was found in more than 800 cases with a steep increase case numbers in early 2014 Zaki et al 2012 de Groot et al 2013 Drosten et al 2014 Clinically MERS CoV presents mainly as a respiratory disease with symptoms ranging from asymptomatic or mild upper respiratory tract disease to severe viral pneumonia and multi organ failure While most confirmed MERS CoV cases originate from the Arabian Peninsula several MERS CoV infections have been imported to Europe United Kingdom Germany Italy France Greece Netherlands Asia Malaysia Philippines and the United States of America Bermingham et al 2012 Drosten et al 2013 Mailles et al 2013 Puzelli et al 2013 Bialek et al 2014 Kraaij Dirkzwager et al 2014 Premila Devi et al 2014 Tsiodras et al 2014 All cases detected outside the Arabian Peninsula were linked to a Middle Eastern country ei ther as a direct result of recent travel or through person to person transmission via a contact case These imported cases highlight the fact that MERS CoV like other airborne viruses such as influenza has the capability for worldwide spread Accepted Article This article is protected by copyright All rights reserved More than 10 million pilgrims from over 184 countries visit the Saudi Arabia KSA annually to perform religious pilgrimages to Mecca and Medina either to perform the annual Hajj pilgrimage which takes place during a certain season or the Umrah Memish et al 2014 With the emergence of MERS CoV on the Arabian Peninsula in 2012 this mass gathering is regarded as a possible trans mission scenario with a risk of international spread of the virus Khan et al 2013 There have been several surveillance studies for MERS CoV in Hajj pilgrims none of which has reported a MERS CoV infection Benkouiten et al 2013 Gautret et al 2013 Rashid et al 2013 Gautret et al 2014 Memish et al 2014 No study on returning pilgrims from KSA to the African con tinent has been conducted although the Muslim community in Africa consists of over 250 million people with about one million annual travels to KSA for the pilgrimage Zumla et al 2014 We pre sent our findings in screening returning pilgrims at Kotoka International airport in Accra Ghana one of West Africa s major intercontinental air travel hubs Materials and methods Study design We conducted a cross sectional surveillance study in November 2013 at the Hajj Village located at the Kotoka International Airport KIA Ghana The Hajj Village is a special arrival destination located on the premises of KIA for all chartered flights from KSA bringing Muslim pilgrims who embarked on the Hajj Pilgrims were enrolled immediately after their return from the Hajj in KSA Our goal was to identify the prevalence of MERS CoV and the common respiratory viruses human Rhinovirus HRV Respiratory Syncytial Virus RSV and Influenza A virus FLU A A standardised questionnaire on demographic and clinical data was completed during a face to face interview Both symptomatic and asymptomatic subjects were recruited Symptomatic subjects were defined as those presenting with any of the following conditions cough sore throat breathing difficulty runny nose sneezing or elevated temperature All symptoms were self reported Asymptomatic subjects did not report any of the symptoms outlined above Sampling Nasopharyngeal specimens were taken with flocked swabs Copan Italy by inserting the swab up the nostril towards the pharynx until resistance was felt Swabs were then rotated 3 times to obtain epithelial cells The swabs were stored in 500 l RNAlater Qiagen Hilden Germany and transport ed to the KCCR laboratory for extraction and testing by real time reverse transcription polymerase chain reaction real time RT PCR Accepted Article This article is protected by copyright All rights reserved Real time RT PCR analysis RNA was purified using a Viral RNA Mini Kit Qiagen according to manufacturer instructions All ex tracts were tested by real time RT PCR using the Qiagen One Step RT PCR System Qiagen and as says with diagnostic sensitivity for HRV Lu et al 2008 RSV Kuypers et al 2004 FLU A Spackman et al 2002 and MERS CoV Corman et al 2012 Corman et al 2012 One Step Real time RT PCR detection was performed on a CFX96 Bio Rad real time PCR platform Bio Rad Singapore In vitro transcribed RNA was used as a positive control In order to include only study subjects with a rele vant viral load for HRV RSV and FLU A only samples with a threshold cycle CT value below 38 were rated as positive and included in our analysis Statistical analysis Study data were double entered into Excel and exported to Stata SE 12 Stata Corporation Texas USA for analysis Pearson s 2 was used to analyse categorical variables where appropriate P values 0 05 were considered significant Ethics consent and approval Approval for this study was obtained from the Public Health Division of the Ghana Health Services GHS Ministry of Health and the Port Health Directorate Kotoka International Airport KIA also un der the GHS All participants were recruited on a voluntary basis The aims and objectives of the study were explained to the pilgrims and verbal consent was obtained before participants were en rolled Results Pilgrimage cohort The cohort consisted of 839 adults recruited for the study in November 2013 The mean participant age was 52 years range 21 to 85 years The male to female ratio was 1 1 2 Table The pilgrims originated from all 10 geographic regions of Ghana with a majority from the Ashanti region 35 8 followed by Greater Accra 22 5 and the Northern Region 20 6 Figure 1 Virus detection Overall 179 21 3 of the 839 screened individuals had a positive finding for at least one of the vi ruses other than MERS HRV was the most common in 141 16 8 individuals RSV in 43 5 1 and FLU A in 11 individuals 1 3 In 16 1 9 pilgrims more than one virus was detected with 14 1 7 RSV HRV and 2 0 2 FLU A HRV co infections Accepted Article This article is protected by copyright All rights reserved Clinical presentation A total 651 77 6 of the pilgrims were symptomatic Both symptomatic and asymptomatic pa tients were of comparable age range and mean age age range 21 to 85 years mean 52 years and age range 22 to 84 years mean 51 years respectively The symptomatic returnees presented with cough 593 91 1 sore throat 343 52 7 el evated temperature 154 23 7 runny nose or sneezing 152 23 3 and breathing difficulty 124 19 0 A total 146 22 4 of the symptomatic returnees tested positive for at least one respiratory virus compared with 33 17 6 of the asymptomatic pilgrims who had at least one detectable virus in their sample 2 06 p 71 35 5 6 15 8 1 Missing 26 4 0 3 1 6 Sex 0 74 0 389 Male 292 44 9 91 48 4 Female 359 55 2 97 51 6 Region of residence 8 59 0 476 Ashanti 226 34 7 74 39 4 Brong Ahafo 25 3 8 7 3 7 Central Region 19 2 9 3 1 6 Eastern Region 16 2 5 1 0 5 Greater Accra 149 22 9 40 21 3 Northern Region 131 20 1 42 22 3 Upper East Region 20 3 0 5 2 7 Upper West Region 32 4 9 12 6 4 Volta 17 2 6 2 1 0 Western Region 16 2 5 2 1 0 Virus detection HRV 114 17 5 27 14 4 1 035 0 31 RSV 36 5 5 7 3 7 0 979 0 32 Flu A 7 1 1 4 2 1 1 249 0 26 Accepted Article This article is protected by copyright All rights reserved